Introduction

Food of animal origin is a relevant source of foodborne diseases; among them, meat is one of the main food vehicles for biological hazards to humans ¹. Due to its physical and chemical characteristics, meat can favor the growth of pathogenic microorganisms such as Salmonella spp., Escherichia coli O157:H7, and other potential foodborne disease carriers or related toxins, which makes meat a food of major risk to public health ^2,3,4 and for which its handling requires adequate safety practices. Indeed, it has been estimated that 14.8% of foodborne disease outbreaks in Colombia were caused by consuming meat and meat products ⁵.

Microbial contamination of meat can occur during the slaughter process, which inevitably takes place in transforming live animals into meat. Most of this contamination comes from dirt, dust, and feces associated with the animal's skin, which encounters the carcass when removed ^6,7.

Several decontamination methods have been reported to reduce the microbial contamination of carcasses: physical (e.g., hot water, steam, steam vacuuming), chemical (e.g., organic acids, chlorine, acidified sodium chlorite, polyphosphates), and biological (e.g., bacteriophages, bacteriocins) ⁸. However, the most effective carcass decontamination techniques are nonbiological, with chemicals, acids, steam, and hot water washes being the most effective ¹.

Chemical decontamination involves the application of a chemical substance at some point during slaughter. The most commonly used and extensively studied substances for chemical decontamination of carcasses are low molecular weight organic acids (e.g., lactic, acetic, citric, fumaric) and other chemicals such as chlorine, acidified sodium chlorite, peroxyacids, and trisodium phosphate ⁸.

Several studies worldwide, including two Colombian studies, have investigated the effect of chemical decontamination and bacterial reduction of beef carcasses ^{9,10,11,12,13}.

Nevertheless, the characterization of decontamination procedures of beef carcasses in abattoirs is scarce, with few studies characterizing these procedures among other food safety practices ^14,15. This lack of reliable information on decontamination procedures of beef carcasses in any country constrains the possibilities for evaluation and improvement, which represents a risk of contamination of meat with pathogenic microorganisms of public health concern ¹⁶. In addition, this undesirable contaminated meat also affects productivity ¹⁷ since the ineffectiveness of microbiological risk control leads to commercial and economic disadvantages for slaughterhouses ^17,18. The decontamination process chosen by the slaughterhouse to guarantee meat safety and reduce the risk of biological hazards must be validated according to government regulations and their preferred methods under specific production conditions and circumstances ^8,19,20.

In 2019, the Colombian cattle slaughter was 3,407,750 heads, of which 96.4% were intended for national consumption. Of this number, the province of Antioquia provided the highest proportion, with 541,003 heads (15.88%) ²¹, making the decontamination characterization procedure highly relevant in this province to reduce the risk of contamination with pathogenic microorganisms of public health concern. Therefore, this study aimed to characterize the decontamination procedures of beef carcasses in slaughterhouses located in the province of Antioquia (Colombia).

Materials and methods

Pre-test of the information collection instruments

All information collection instruments -questionnaires and forms, were pre-tested at a small scale to evaluate their effectiveness. In each case (i.e., documentary review from the Invima´s TWG Occidente 1 repository, characterization information of each slaughterhouse during the visit, and characterization of the routine decontamination procedure during the visit). Six experts in the field (one doctor of engineering and five veterinarians with long experience in beef abattoirs and postgraduate studies in the field of veterinary public health) evaluated the structure to ensure that all important issues were identified and covered, and to identify problems, such as unnecessary length, poorly worded, unclear questions, or allowance of subjective responses ²³ (Figure 1).

Figure 1 General information on the study design for the characterization of beef carcass decontamination procedure at slaughterhouse in the province of Antioquia (Colombia), 2019-2021. 

Results

Discussion

The current study characterized the beef carcass decontamination procedures routinely used in slaughterhouses. The response rate obtained was lower (52%) when compared to similar studies using comparable methodologies ^14,15. Although several efforts were made to increase the response, the voluntary participation in the research and some pre-existing prejudice against sharing information on safety procedures with academia led to the response rate obtained.

The five slaughterhouses that did not have a permanent official inspection could get access to this critical inspection service provided by territorial entities taking advantage of the regulations and guidelines issued by the Ministry of Health and Social Protection ^24,25) similar to the inspection system of other countries, such as Mexico, USA, and Canada, with federal and state inspection ^14,26,27,28. Some authors have suggested a relationship between the reduction in the prevalence of pathogens in the final product and access to an official inspection, resulting in microbiologically safer carcasses ²⁶.

More than 90% of the slaughterhouses were small and/or very small plants, similar to others found in previous studies ^14,15,27,28. It was hypothesized that slaughterhouses with higher slaughter volumes -at least 80,000 cattle/year (6,700 cattle/month), can invest in aspects related to ensuring product safety, as suggested by other studies ^14,27. Due to their size, very small slaughterhouses have a low income and limited financial resources, so they save on aspects such as performing validation studies of the decontamination process used, acquiring technological resources such as automated intervention systems, and training personnel.

According to national health regulations, the personnel responsible for the operation must understand and conduct the activities under their responsibility ^3,29. Continuous training in aspects associated with carcass decontamination should be reinforced in slaughterhouses since personnel training is essential to produce safe food ^15,30.

The use of chemical products such as citric acid, lactic acid, peracetic acid, and a mixture of organic acids in carcass decontamination has also been identified by other researchers for the control of pathogenic microorganisms in meat ^31,32,33,34. Although the substances used in the decontamination process vary between slaughterhouses, sprinkling organic acids was also evidenced in a previous study ¹⁴.

According to our results, citric acid is the most commonly used product at concentrations between 900 and 1,500 ppm (0.09-0.15%), which is consistent with the product's technical data sheet (i.e., 900-3,000 ppm). However, the concentrations at which the product was being applied were well below, compared to other studies, where 2% citric acid was not enough to significantly reduce pathogens ^34,35. In the current study, it was established that three of the 12 slaughterhouses visited applied lactic acid at concentrations between 1.2 and 2%; however, previous research has recommended the use of lactic acid at concentrations between 2 and 4% to obtain reductions greater than one logarithmic unit ^6,27,31.

Three of the studied slaughterhouses used peracetic acid at concentrations between 160 and 210 ppm, which is the recommended maximum concentration of 220 ppm ³⁶. However, another study reports that it is not an effective intervention according to what is recognized ³⁵.

It was identified that in most of the slaughterhouses of the study, the method of application of the decontamination product was manual. This type of application is less effective in reducing microbial populations ³⁴. Considering that most of the slaughterhouses in Antioquia are small or very small -many in the latter classification, it is unlikely that the automated application mode was one of the most used since the latter is more suitable for larger slaughterhouses slaughter volumes ¹⁵. One explanation is the cost of such equipment and production needs, which makes it more likely to be used by larger slaughterhouses since they have more resources to implement these technologies.

In most of the slaughterhouses visited, it was observed that the operator responsible for the carcass decontamination procedure is not exclusively responsible for conducting this activity, which may increase fatigue. In addition, during the direct observation of the decontamination procedure, the slaughterhouses indicated that they were unaware of the disinfectant volume and application pressure. Other research has reported volumes ranging from 250 to 473 mL per carcass ³⁷, and better results have been reported when using 2 to 3 L per carcass ³⁴ and an application pressure range between 10-123 psi ^18,38. Therefore, and in accordance with what has been pointed out in other studies, in addition to the concentration of the disinfectant, several specific variables of the process must be controlled, such as operator fatigue, pressure or lack of spraying of the product, the volume of the disinfectant applied, time of exposure to the disinfectant, and coverage area of the carcass with the spray, since these factors significantly influence the efficacy of carcass decontamination treatments ^31,34,41.

According to what was observed, most of the slaughterhouses in the study have implemented an intervention method to control pathogenic microorganisms. In Antioquia, the most used method is washing carcasses with water at room temperature (average 19.9 °C) and sprinkling organic acids. Although it is recognized and accepted that an intervention is effective when it achieves at least a logarithmic reduction ²⁷, and although the effectiveness of this decontamination procedure has been demonstrated, washing with water at room temperature and spraying with organic acids is the least effective alternative since it reduces only 1 to 1.5 logarithmic units ^27,39. Hot water carcass washing was not used in the slaughterhouses study, an intervention that, like chemical disinfection, has increased over time as a pathogen control strategy in the US ¹⁵. Other studies have found that the combination of hot water washing (<55 °C) followed by organic acid spraying resulted in additional reductions of 0.2 to 0.5 and of 0.5 to 1.9 log units for E. coli O157: H7 and S. typhimurium, respectively, which are pathogenic bacteria of interest in meat ^6,35,15,40. Furthermore, this strategy could reduce the bacterial load due to cross-contamination and is suggested for small and very small slaughterhouses ²⁶. Therefore, it is considered a viable alternative to improve the conditions of the carcass decontamination procedures, according to the features of the slaughterhouses located in the province of Antioquia.

As discussed above and considering that none of the slaughterhouses visited acknowledge implementing the multi-barrier strategy -including a good preventive intervention such as supplier control, the multi-barrier approach significantly improves results and is more effective than a single intervention is used ^14,41,42. Combining washing with hot water (<55 °C) followed by spraying with organic acids would be a practical and acceptable option for slaughterhouses in Antioquia.

Most of the slaughterhouses visited carried out a microbiological sampling of the carcasses to verify the effectiveness of the decontamination procedure, an aspect required according to Colombian health regulations ^3,29. However, process control could be improved and monitored through well-designed sampling plans. Therefore, it is agreed to state that although the good manufacturing practices are essential for properly carrying out the slaughter process, pathogen sampling and control plans can help filter contaminated products during the transformation process, stimulate improvements in cleaning and disinfection procedures, and reduce consumer risk and financial costs associated with rejected products by improving product safety ⁴³. In addition, to achieve control of pathogens in carcasses, sanitary standards require the interventions used to destroy and prevent the growth of pathogens to be validated under manufacturing conditions ^3,29. Therefore, it is recommended that the beef carcass decontamination procedure chosen by the slaughterhouses must be validated under the local environments and conditions of each one, as has been recommended in other research works ^11,41.

Conclusion

Although it was established that at least one decontamination procedure, such as chemical disinfection, is implemented in the slaughterhouses of study, this option is not supported by scientific or technical foundations. It is likely that, due to limited resources or low income, slaughterhouses are saving on technical factors, technology, and staff training and suitability. These findings support the need for improvements in the slaughterhouses of the province of Antioquia, including the improvement of surveillance programs to effectively reduce pathogens in the meat chain.